INSIGHT
DECISION MAKING
Hitting an uncertain target
Experiments in which monkeys have to select or estimate the location of
a target are revealing more about the role of the dorsal premotor cortex
in decision making.
VEIT STUPHORN
Related research article Dekleva BM,
Ramkumar R, Wanda PA, Kording KP, Miller LE.
2016. Uncertainty leads to persistent effects on
reach representations in dorsal premotor
cortex. eLife 5:e14316. doi: 10.7554/eLife.
14316
Image Maps of neural activity in the dorsal
premotor cortex (left) and the primary motor
cortex (right)
L
Copyright Stuphorn. This article is
distributed under the terms of the
Creative Commons Attribution
License, which permits unrestricted
use and redistribution provided that
the original author and source are
credited.
ife is full of uncertainty. Take, for example, a football player preparing to take a
penalty kick. He or she can aim to kick the
ball along a number of different trajectories, and
the success of the kick will depend on a range of
different factors, such as small differences in the
execution of the kick and, most importantly, the
response of the goalkeeper. The simplest way to
think about the decision that the player has to
make is to say that he or she has to decide
between two options: aiming for the left half of
the goal or aiming for the right half (Figure 1A).
Most studies of the neuronal mechanisms that
underlie decision-making have focused on "target selection" situations like this, where the
available options are limited in number and
clearly distinct from each other (Shadlen and
Newsome, 2001; Romo et al., 2004; Thura and
Cisek, 2014).
However, the player taking the penalty obviously has more than two options: they can, for
example, aim low, which increases their chances
of hitting the goal, but also gives the goalkeeper
Stuphorn. eLife 2016;5:e18721. DOI: 10.7554/eLife.18721
a better chance to make a save; or they can aim
high to make it more difficult for the goalkeeper
and themselves. Indeed, they can aim at any
point in the goal. This means that the player has
to decide between an infinitely large range of
possible trajectories (Figure 1B). To do this, he
or she has to estimate the probability of success
for each possible trajectory and then select the
one with the highest likelihood of success. In the
language of neuroscience the player is confronted with a "target estimation" situation.
How might the brain make a decision in such
a situation? Studies of primates suggest that a
region of the brain called the dorsal premotor
cortex plays an important role in making target
selection decisions (Cisek and Kalaska, 2005),
and that the primary motor cortex is responsible
for executing such decisions. Now, in eLife, Lee
Miller and colleagues at Northwestern University, including Brain Dekleva as first author,
report the results of experiments on monkeys
that shed new light on the role of these two
regions in making target estimation decisions
(Dekleva et al., 2016). The experiments
involved simultaneously recording neural activity
in the dorsal premotor cortex and the primary
motor cortex as the monkeys performed a target
estimation task.
Playing football would be impractical in an
electrophysiological experiment so, instead, two
monkeys were trained to use a device called a
manipulandum to move a cursor on a screen. The
experiment involved two types of trials. During
the first type of trial the monkey held the cursor
over a central target: then, after a random period
of time, the central target disappeared and a new
target appeared in one of eight locations (which
were arranged in a circle around the central
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Insight
Decision making Hitting an uncertain target
Figure 1. Target selection and target estimation. (A) In a target selection situation there is a choice between two
or more, clearly distinct, options. In this example there are two options (indicated by the two red arrows), and each
option is associated with a specific probability of success (indicated by the numbers). A region of the brain called
the dorsal premotor cortex plays an important role in making target selection decisions (also known as categorical
decisions), while the primary motor cortex is responsible for executing the decision. (B) In a target estimation
situation there is an infinite number of options (six of which are indicated by red arrows), and the probability of
success can be plotted as a distribution with two peaks (yellow line). (C) Dekleva et al. have performed
experiments on monkeys to explore the roles played by the dorsal premotor cortex and the primary motor cortex
in making target estimation decisions (also known as continuous decisions). In the experiments the monkeys had
to select a specific direction from a range of possible directions on the basis of incomplete visual information.
Dekleva et al. measured how the level of neural activity (y-axis) in these two regions of the brain varied as a
function of the angle (x-axis) between the preferred direction of the neurons and the chosen direction; they also
varied the degree of uncertainty in the visual information provided to the monkeys about the location of the
target. The range of possible directions was wide (orange arrows) when the uncertainty in the visual information
provided to the monkeys was high, and the range was narrow (green arrows) when the uncertainty was low. In
both regions the level of neural activity was highest when the angle between the preferred direction and the
chosen direction (indicated by the vertical arrow) was zero. However, high levels of neural activity were observed
over a relatively wide range of angles in the dorsal premotor cortex (left inset), and this range was higher when the
degree of uncertainty was higher (orange line). In the primary motor cortex, on the other hand, high levels of
neural activity were only observed for a narrow range of directions around the chosen direction, independent of
the degree of uncertainty in the visual information (right inset).
target). The monkey received a reward every
time it moved the cursor to the correct target.
Neurons in the dorsal premotor cortex (PMd neurons) and the primary motor cortex have a "preferred direction", and the Northwestern group
measured the level of neural activity as a function
of the angle between the preferred direction of
groups of neurons and the direction selected by
the monkey (Figure 1C).
Stuphorn. eLife 2016;5:e18721. DOI: 10.7554/eLife.18721
During the second type of trial the location of
the new target was indicated by number of small
lines that were sampled from a distribution that
was centered on the target location. (There were
five small lines for one monkey, ten for the
other). The lines supplied the monkeys with
incomplete information about the target location, and Dekleva et al. were able to vary the
degree of uncertainty in this information by
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Insight
Decision making Hitting an uncertain target
varying the width of the distribution from which
the lines were sampled. This meant that the
monkeys were now performing a target estimation task.
When the degree of uncertainty in the visual
information supplied to the monkeys was high
they tended to move the cursor to a location
that was the average of the target locations in
the previous trials: this approach makes sense
when relatively little information is available. The
Northwestern group also observed relatively
high levels of activity in the PMd neurons representing directions other than the selected direction when the uncertainty was high: this
suggests that, during decision making, the dorsal premotor cortex represents all directions that
might be correct, each weighted by its probability of success. Again this makes sense: when the
degree of uncertainty is high, there is a higher
likelihood that a direction other than the chosen
one is correct, so the PMd neurons representing
these other directions are more active. In contrast, in the primary motor cortex, only those
neurons representing the chosen direction were
active (Figure 1C).
Previous studies of target selection reported
that the activity of PMd neurons representing
the chosen action increased during decision
making, whereas the activity of other PMd neurons decreased (Cisek and Kalaska, 2005;
Thura and Cisek, 2014). This was taken as evidence that the dorsal premotor cortex plays a
direct role in decision making. In contrast, by
showing that the PMd neurons representing all
possible actions are active throughout the planning and execution of a target estimation task,
the results of the Northwestern team argue
strongly against a direct role for the dorsal premotor cortex in decision making because it is
the M1 neurons, but not the PMd neurons, that
encode the chosen direction unambiguously.
Future experiments should compare the role
of PMd neurons in both target selection and target estimation tasks. Examining situations that
are intermediate between target selection and
target estimation might also help to resolve the
difference between the latest findings and previous work.
The latest results also shed some light on the
question how probability and uncertainty are
encoded in the brain. There is some evidence
for an explicit representation of uncertainty in
the orbitofrontal cortex of primates (O’Neill and
Stuphorn. eLife 2016;5:e18721. DOI: 10.7554/eLife.18721
Schultz, 2010). However, recent work in rodents
indicates that other interpretations are possible
(Ogawa et al., 2013), and the results of Dekleva
et al. support an implicit (rather than explicit)
representation (Ma et al., 2006).
By pioneering the study of an important class
of real-world situations that have been
neglected up to now, the work of the Northwestern group opens up a rich new field of
investigation.
Veit Stuphorn is in the Department of Psychological
and Brain Sciences, Johns Hopkins University,
Baltimore, United States and the Department of
Neuroscience and the Krieger Mind/Brain Institute,
Johns Hopkins School of Medicine, Baltimore, United
States
veit@jhu.edu
http://orcid.org/0000-0003-1117-9993
Competing interests: The author declares that
no competing interests exist.
Published 15 July 2016
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